Place Field-Memory Field Unity of Hippocampal Neurons

Hippocampal principal neurons display both spatial tuning properties and memory features. Whether this distinction corresponds to unique neuron types or a context-dependent continuum has been debated. We report here that the task-context (“splitter”) feature is highly variable along both trial and spatial position axes. Neurons acquired or lost splitter features across trials even when place field features remain unaltered. Multiple place fields from the same neuron could individually encode both past or future run trajectories, implying that splitter fields are under the control of assembly activity, which we confirm with population vector analysis. Even typical place fields can be differentiated into subfields by the behavioral choice of the animal and splitting subfields can evolve even within a single place field. A fraction of interneurons also differentiated left and right choices by integrating inputs from their partner pyramidal cells. Finally, bilateral optogenetic inactivation of the medial entorhinal cortex reversibly decreased the fraction of splitter fields. Our findings suggest that place or splitter features are different manifestations of the same hippocampal computation.